The interactive roles of nutrient loading and zooplankton grazing in facilitating the expansion of harmful algal blooms caused by the pelagophyte,Aureoumbra lagunensis,to the Indian River Lagoon,FL, USA

Confined to Texas, USA, for more than 20 years, brown tides caused by Aureoumbra lagunensis emerged in the Indian River Lagoon and Mosquito Lagoon, Florida, USA, during 2012 and 2013, affording the opportunity to assess whether hypotheses developed regarding the occurrence of these blooms are ecosystem-specific. To examine the extent to which top-down (e.g. grazing) and bottom-up (e.g. nutrients) processes controlled the development of Aureoumbra blooms in Florida, nitrogen (N) uptake, nutrient amendment, and seawater-dilution, zooplankton grazing experiments were performed and the responses of Aureoumbra and competing phytoplankton were evaluated. During the study, Aureoumbra comprised up to 98% of total phytoplankton biomass, achieved cell densities exceeding 2 × 10⁶ cells mL⁻¹, and contained isotopically lighter N compared to non-bloom plankton populations, potentially reflecting the use of recycled N. Consistent with this hypothesis, N-isotope experiments revealed that urea and ammonium accounted for >90% of N uptake within bloom populations whereas nitrate was a primary N source for non-bloom populations. Low levels (10 μM) of experimental ammonium enrichment during blooms frequently enhanced the growth of Aureoumbra and resulted in the growth rates of Aureoumbra exceeding those of phycoerythrin-containing, but not phycocyanin-containing, cyanobacteria. A near absence of grazing pressure on Aureoumbra further enabled this species to out-grow other phytoplankton populations. Given this alga is generally known to resist zooplankton grazing under hypersaline conditions, these findings collectively suggest that moderate loading rates of reduced forms of nitrogenous nutrients (e.g ammonium, urea) into other subtropical, hypersaline lagoons could make them susceptible to future brown tides caused by Aureoumbra.     

3,000 km and 1,500‐year presence of Aureococcus anophagefferens reveals indigenous origin of brown tides in China

The nonmotile, spherical, picoplanktonic (2‐μm‐sized) pelagophyte Aureococcus anophagefferens has caused numerous harmful blooms (“brown tides”) across global marine ecosystems. Blooms have developed along the east coast of the USA since 1985, a limited number of times in South Africa around 1997, and frequently in China since 2009. As a consequence, the harmful blooms have caused massive losses in aquaculture and coastal ecosystems, particularly mortalities in cultured shellfish. Therefore, whether A. anophagefferens was recently introduced to China via natural/artificial transport of resting stage cells or has been an indigenous species has become a question of profound ecological significance and broad interest, which motivated our extensive investigation on the geographic and historical presence of this species in the seas of China. We applied a combined approach of extensive PCR‐based detection and sequencing, germination experiments and monoclonal antibody staining of germlings to samples of surface sediment and sediment core (dated via combined isotopic measurements) collected from all four seas of China, and searched the supplementary data set of a recent Science publication. We discovered that A. anophagefferens does have a resting stage in the sediment, but it also has a wide geographic distribution both in China (covering a range of ~30° in latitude, ~15.7° in longitude and 2.5–3,456 m in water depth; temperate to tropical and coastal to open oceans) and in almost all oceans of the world and a historical presence of >1,500 years in the Bohai Sea, China. The work revealed that A. anophagefferens is not a recently introduced, but an indigenous species in China and has in fact a globally cosmopolitan distribution.     

Sexual resting cyst production by the dinoflagellate Akashiwo sanguinea: a potential mechanism contributing to the ubiquitous distribution of a harmful alga

The dinoflagellate Akashiwo sanguinea is a well known, cosmopolitan harmful microalga that frequently forms harmful algal blooms (HABs) in marine estuaries from temperate to tropical waters, and has posed a severe threat to fish, shellfish, and sea birds. Therefore, it is important to understand the ecology of this species, particularly the mechanisms regulating its ubiquitous geographic distribution and frequent recurrence of. To date, the mechanisms regulating distribution and recurrence of HABs by this species have been poorly understood. While resting cyst production can play a central role in the geographic expansion and initiation of HABs, studies of the life cycle of this alga, including cyst production, have been lacking. Here, we demonstrate that A. sanguinea produces sexual resting cysts homothallically. We present evidence for cell pairs in sexual mating, biflagellated planozygote formation, and cysts of different morphologies, and we describe time series for germination of cysts to germlings with two longitudinal flagella, along with studies of possible factors affecting cyst production. Phylogenetic analysis of large sub‐unit rDNA sequences revealed a monophyly of this species and thus possibly a recent common ancestor for all global populations. The discovery of resting cyst production by A. sanguinea suggests its frequent recurrence of blooms and global distribution may have been facilitated by the natural and anthropogenic transport of resting cysts.     

Organic and inorganic nutrient effects on growth rate–irradiance relationships in the Texas brown‐tide alga Aureoumbra lagunensis (Pelagophyceae)1

Pelagophyte species in the genera Aureococcus and Auroumbra form brown tides in coastal bays that cause food‐web disruption and extensive shading of benthic primary producers. Organic nutrients have been suggested as key factors in the origination and persistence of the East Coast (USA) brown‐tide alga Aureococcus anophagefferens Hargraves et Sieburth. To evaluate this finding for the Texas brown‐tide alga Aureoumbra lagunensis D. A. Stockw., DeYoe, Hargraves et P. W. Johnson, we grew strain TBA‐2 with dissolved inorganic nitrogen (DIN; or ) or dissolved organic nitrogen (DON; urea or glutamate) as the nitrogen (N) source under eight light intensities. Maximum growth rates decreased with N source from (1.0 div · d^?1) to (0.48 div · d^?1). Neither growth rate efficiency (α) nor I_k varied significantly between N treatments. Both inorganic phosphorus (P) and β‐glycerophosphate supported growth. Aureoumbra lagunensis can utilize at least some forms of organic N and P and can use them to persist or grow when inorganic forms become limiting. We found no evidence to support the hypothesis that organic utilization enhances or supplements growth at low light levels.     

Development of microsatellite markers for the red tide‐forming harmful species Chattonella antiqua,C. marina,and C. ovata (Raphidophyceae)

We have developed 11 microsatellite markers that are specific to Chattonella antiqua, C. marina, and C. ovata, the red tide‐forming harmful phytoplanktons. The 11 loci were amplified in the three species. The number of alleles per locus ranged from 5 to 16. The three species shared most microsatellite regions, although the genetic differences in specific loci were detected among them. These markers of the Chattonella species will be beneficial for biogeographical, detailed taxonomic, studies.     

First reports of Pseudo‐nitzschia micropora and P. hasleana (Bacillariaceae) from the Southern Hemisphere: Morphological,molecular and toxicological characterization

Pseudo‐nitzschia H. Peragallo is a marine diatom genus found worldwide in polar, temperate, subtropical and tropical waters. It includes toxigenic representatives that produce domoic acid (DA), a neurotoxin responsible for Amnesic Shellfish Poisoning. In this study we characterized two species of Pseudo‐nitzschia collected from Port Stephens and the Hawkesbury River (south eastern Australia) previously unreported from Australian waters. Clonal isolates were sub‐sampled for (i) light and transmission electron microscopy; (ii) DNA sequencing, based on the nuclear‐encoded partial large subunit ribosomal RNA gene and internal transcribed spacer (ITS)‐ITS1, 5.8S and ITS2 rDNA regions and, (iii) DA production as measured by liquid chromatography‐mass spectrometry. Morphological and molecular data unambiguously revealed the species to be Pseudo‐nitzschia micropora Priisholm, Moestrup & Lundholm (Port Stephens) and Pseudo‐nitzschia hasleana Lundholm (Hawkesbury River). This is the first report of the occurrence of these species from the Southern Hemisphere and the first report of P. micropora in warm‐temperate waters. Cultures of P. micropora, tested for DA production for the first time, proved to be non‐toxic. Similarly, no detectable toxin concentrations were observed for P. hasleana. Species resolution and knowledge on the toxicity of local Pseudo‐nitzschia species has important implications for harmful algal bloom monitoring and management.     

Cuticular hydrocarbons as a basis for chemosensory self‐referencing in crickets: a potentially universal mechanism facilitating polyandry in insects

Females of many species obtain benefits by mating polyandrously, and often prefer novel males over previous mates. However, how do females recognise previous mates, particularly in the face of cognitive constraints? Female crickets appear to have evolved a simple but effective solution: females imbue males with their own cuticular hydrocarbons (CHCs) at mating and utilise chemosensory self‐referencing to recognise recent mates. Female CHC profiles exhibited significant additive genetic variation, demonstrating that genetically unique chemical cues are available to support chemosensory self‐referencing. CHC profiles of males became more similar to those of females after mating, indicating physical transfer of CHCs between individuals during copulation. Experimental perfuming of males with female CHCs resulted in a female aversion to males bearing chemical cues similar to their own. Chemosensory self‐referencing, therefore, could be a widespread mechanism by which females increase the diversity of their mating partners.     

Phylogeographic characteristics of hypervariable regions in the mitochondrial genome of a cosmopolitan,bloom‐forming raphidophyte,Heterosigma akashiwo

The global distribution of phytoplankton is defined by many events, including long‐term evolutionary processes and shorter time span processes (e.g., global climate change). Furthermore, human‐assisted, unintentional dispersion, including the transport of live fish and spat for aquaculture, and transfer of aquatic microorganisms contained in ship ballast water, may aid the spread of phytoplankton. To understand the phylogeographic history of a species, the development of useful molecular markers is crucial. We previously reported a hypervariable mitochondrial gene in the cosmopolitan bloom‐forming alga, Heterosigma akashiwo. In this study, we identified two additional hypervariable segments in the H. akashiwo mitochondrial genome, one a protein coding sequence, and the other an intergenic region, by comparing the whole mitogenomes of strains obtained from various geographic origins. Interestingly, the newly identified hypervariable protein coding sequence was a paralogue of the previously identified gene, and both sequences showed tendencies to correlate with latitude of geographic origin. However, the hypervariable intergenic sequence did not show a clear correlation with origin. Our results demonstrated that the protein coding sequences may serve as useful tools for understanding the phylogeographic history of H. akashiwo, and they may crucially function in adaptation of the species to the environment.     

Field experiments on mitigation of harmful algal blooms using a Sophorolipid—Yellow clay mixture and effects on marine plankton

This study examined a new method of mitigating harmful algal blooms (HABs) by combining biosurfactant sophorolipid and yellow clay. To investigate the effects and practicability of this HAB mitigation method, field experiments were carried out during a Cochlodinium bloom near Miruk Island, South Korea, in August 2002. Field experiments examined the effects of sophorolipid and yellow clay on Cochlodinium bloom mitigation and on marine plankton such as bacteriaplankton, heterotrophic protists, and zooplankton. A mixture of 5 mg l⁻¹ sophorolipid and 1 g l⁻¹ yellow clay was sprayed directly on the sea surface and its effect was compared with that of 10 g l⁻¹ of yellow clay applied under similar conditions. The sophorolipid–yellow clay mixture more efficiently mitigated the Cochlodinium bloom (95% removal efficiency after 30 min) than yellow clay alone (79% after 30 min). Further, no variation in bacterial abundance occurred 30 min after spraying the sophorolipid–yellow clay mixture. After 30 min, heterotrophic protist abundance at the surface decreased 21 and 41%, respectively, following the sophorolipid–yellow clay mixture and yellow clay treatments. Zooplankton decreased by 38% 15 min after spraying the mixture and 67% 30 min after spraying the yellow clay. These results indicate that the mixture of sophorolipid and yellow clay had a less adverse effect on bacteriaplankton, heterotrophic protists, and zooplankton than the yellow clay, suggesting that the sophorolipid–yellow clay mixture can mitigate HABs efficiently with fewer negative effects on the pelagic ecosystem.     

Mixotrophy in the phototrophic harmful alga Cochlodinium polykrikoides (Dinophycean): prey species, the effects of prey concentration, and grazing impact

We first reported here that the harmful alga Cochlodinium polykrikoides, which had been previously known as an autotrophic dinoflagellate, was a mixotrophic species. We investigated the kinds of prey species and the effects of the prey concentration on the growth and ingestion rates of C. polykrikoides when feeding on an unidentified cryptophyte species (Equivalent Spherical Diameter, ESD = 5.6 microm). We also calculated grazing coefficients by combining field data on abundances of C. polykrikoides and co-occurring cryptophytes with laboratory data on ingestion rates obtained in the present study. Cocholdinium polykrikoides fed on prey cells by engulfing the prey through the sulcus. Among the phytoplankton prey offered, C. polykrikoides ingested small phytoplankton species that had ESD's < or = 11 microm (e.g. the prymnesiophyte Isochrysis galbana, an unidentified cryptophyte, the cryptophyte Rhodomonas salina, the raphidophyte Heterosigma akashiwo, and the dinoflagellate Amphidinium carterae). It did not feed on larger phytoplankton species that had ESD's > or = 12 microm (e.g. the dinoflagellates Heterocapsa triquetra, Prorocentrum minimum, Scrippsiella sp., Alexandrium tamarense, Prorocentrum micans, Gymnodinium catenatum, Akashiwo sanguinea, and Lingulodinium polyedrum). Specific growth rates of C. polykrikoides on a cryptophyte increased with increasing mean prey concentration, with saturation at a mean prey concentration of approximately 270 ng C ml(-1) (i.e. 15,900 cells ml(-1)). The maximum specific growth rate (mixotrophic growth) of C. polykrikoides on a cryptophyte was 0.324 d(-1), under a 14:10 h light-dark cycle of 50 microE m(-2) s(-1), while its growth rate (phototrophic growth) under the same light conditions without added prey was 0.166 d(-1). Maximum ingestion and clearance rates of C. polykrikoides on a cryptophyte were 0.16 ng C grazer(-1)d(-1) (9.4 cells grazer(-1)d(-1)) and 0.33 microl grazer(-1)h(-1), respectively. Calculated grazing coefficients by C. polykrikoides on cryptophytes were 0.001-0.745 h(-1) (i.e. 0.1-53% of cryptophyte populations were removed by a C. polykrikoides population in 1 h). The results of the present study suggest that C. polykrikoides sometimes has a considerable grazing impact on populations of cryptophytes.     

Reproductive mode evolution in lizards revisited: updated analyses examining geographic,climatic and phylogenetic effects support the cold‐climate hypothesis

Viviparity, the bearing of live young, has evolved well over 100 times among squamate reptiles. This reproductive strategy is hypothesized to allow maternal control of the foetus' thermal environment and thereby to increase the fitness of the parents and offspring. Two hypotheses have been posited to explain this phenomenon: (i) the cold‐climate hypothesis (CCH), which advocates low temperatures as the primary selective force; and (ii) the maternal manipulation hypothesis (MMH), which advocates temperature variability as the primary selective force. Here, we investigate whether climatic and geographic variables associated with the CCH vs. the MMH best explain the current geographical distributions of viviparity in lizards while incorporating recent advances in comparative methods, squamate phylogenetics and geospatial analysis. To do this, we compared nonphylogenetic and phylogenetic models predicting viviparity based on point‐of‐capture data from 20 994 museum specimens representing 215 lizard species in conjunction with spatially explicit bioclimatic and geographic (elevation and latitude) data layers. The database we analysed emphasized Nearctic lizards from three species‐rich genera (Phrynosoma, Plestiodon and Sceloporus); however, we additionally analysed a less substantial, but worldwide sample of species to verify the universality of our Nearctic results. We found that maximum temperature of the warmest month (and, less commonly, elevation and maximum temperature of the driest quarter) was frequently the best predictor of viviparity and showed an association consistent with the CCH. Our results strongly favour the CCH over the MMH in explaining lizard reproductive mode evolution.     

Clonal expansion of mitochondrial DNA deletions is a private mechanism of aging in long‐lived animals

Disruption of mitochondrial metabolism and loss of mitochondrial DNA (mtDNA) integrity are widely considered as evolutionarily conserved (public) mechanisms of aging (López‐Otín et al., Cell, 153, 2013 and 1194). Human aging is associated with loss in skeletal muscle mass and function (Sarcopenia), contributing significantly to morbidity and mortality. Muscle aging is associated with loss of mtDNA integrity. In humans, clonally expanded mtDNA deletions colocalize with sites of fiber breakage and atrophy in skeletal muscle. mtDNA deletions may therefore play an important, possibly causal role in sarcopenia. The nematode Caenorhabditis elegans also exhibits age‐dependent decline in mitochondrial function and a form of sarcopenia. However, it is unclear if mtDNA deletions play a role in C. elegans aging. Here, we report identification of 266 novel mtDNA deletions in aging nematodes. Analysis of the mtDNA mutation spectrum and quantification of mutation burden indicates that (a) mtDNA deletions in nematode are extremely rare, (b) there is no significant age‐dependent increase in mtDNA deletions, and (c) there is little evidence for clonal expansion driving mtDNA deletion dynamics. Thus, mtDNA deletions are unlikely to drive the age‐dependent functional decline commonly observed in C. elegans. Computational modeling of mtDNA dynamics in C. elegans indicates that the lifespan of short‐lived animals such as C. elegans is likely too short to allow for significant clonal expansion of mtDNA deletions. Together, these findings suggest that clonal expansion of mtDNA deletions is likely a private mechanism of aging predominantly relevant in long‐lived animals such as humans and rhesus monkey and possibly in rodents.     

A novel approach to parasite population genetics: Experimental infection reveals geographic differentiation,recombination and host‐mediated population structure in Pasteuria ramosa,a bacterial parasite of Daphnia

The population structure of parasites is central to the ecology and evolution of host‐parasite systems. Here, we investigate the population genetics of Pasteuria ramosa, a bacterial parasite of Daphnia. We used natural P. ramosa spore banks from the sediments of two geographically well‐separated ponds to experimentally infect a panel of Daphnia magna host clones whose resistance phenotypes were previously known. In this way, we were able to assess the population structure of P. ramosa based on geography, host resistance phenotype and host genotype. Overall, genetic diversity of P. ramosa was high, and nearly all infected D. magna hosted more than one parasite haplotype. On the basis of the observation of recombinant haplotypes and relatively low levels of linkage disequilibrium, we conclude that P. ramosa engages in substantial recombination. Isolates were strongly differentiated by pond, indicating that gene flow is spatially restricted. Pasteuria ramosa isolates within one pond were segregated completely based on the resistance phenotype of the host—a result that, to our knowledge, has not been previously reported for a nonhuman parasite. To assess the comparability of experimental infections with natural P. ramosa isolates, we examined the population structure of naturally infected D. magna native to one of the two source ponds. We found that experimental and natural infections of the same host resistance phenotype from the same source pond were indistinguishable, indicating that experimental infections provide a means to representatively sample the diversity of P. ramosa while reducing the sampling bias often associated with studies of parasite epidemics. These results expand our knowledge of this model parasite, provide important context for the large existing body of research on this system and will guide the design of future studies of this host‐parasite system.     

Interactions between metazoans,autotrophs, mixotrophs and bacterioplankton in nutrient‐depleted high DOC environments: a long‐term experiment

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Florida red tide and brevetoxins: Association and exposure in live resident bottlenose dolphins (Tursiops truncatus) in the eastern Gulf of Mexico,U.S.A.

Bottlenose dolphins (Tursiops truncatus) along the Gulf of Mexico are frequently exposed to blooms of the toxic alga, Karenia brevis, and brevetoxins associated with these blooms have been implicated in several dolphin mortality events. Studies on brevetoxin accumulation in dolphins have typically focused on analyses of carcasses from large‐scale die‐offs; however, data are scarce for brevetoxin loads in live individuals frequently exposed to K. brevis blooms. This study investigated in vivo brevetoxin exposure in free‐ranging bottlenose dolphins resident to Sarasota Bay, Florida, utilizing samples collected during health assessments performed during multiple K. brevis blooms occurring from 2003 to 2005. Brevetoxins were detected by ELISA and LC‐MS in 63% of bottlenose dolphins sampled (n= 30) concurrently with a K. brevis bloom. Brevetoxins were present in urine and gastric samples at concentrations ranging from 2 to 9 ng PbTx‐3 eq/g, and in feces at concentrations ranging from 45 to 231 ng PbTx‐3 eq/g. Samples from individuals (n= 12) sampled during nonbloom conditions (≤1,000 cells/L) were negative for brevetoxin activity. Brevetoxin accumulation data from this study complement dolphin carcass and prey fish data from the same study area, and aid in evaluating impacts of harmful algal blooms on sentinel marine animal species along the west Florida coast.     

Entanglement is a costly life‐history stage in large whales

Individuals store energy to balance deficits in natural cycles; however, unnatural events can also lead to unbalanced energy budgets. Entanglement in fishing gear is one example of an unnatural but relatively common circumstance that imposes energetic demands of a similar order of magnitude and duration of life‐history events such as migration and pregnancy in large whales. We present two complementary bioenergetic approaches to estimate the energy associated with entanglement in North Atlantic right whales, and compare these estimates to the natural energetic life history of individual whales. Differences in measured blubber thicknesses and estimated blubber volumes between normal and entangled, emaciated whales indicate between 7.4 × 10¹⁰ J and 1.2 × 10¹¹ J of energy are consumed during the course to death of a lethal entanglement. Increased thrust power requirements to overcome drag forces suggest that when entangled, whales require 3.95 × 10⁹ to 4.08 × 10¹⁰ J more energy to swim. Individuals who died from their entanglements performed significantly more work (energy expenditure × time) than those that survived; entanglement duration is therefore critical in determining whales’ survival. Significant sublethal energetic impacts also occur, especially in reproductive females. Drag from fishing gear contributes up to 8% of the 4‐year female reproductive energy budget, delaying time of energetic equilibrium (to restore energy lost by a particular entanglement) for reproduction by months to years. In certain populations, chronic entanglement in fishing gear can be viewed as a costly unnatural life‐history stage, rather than a rare or short‐term incident.